Download Flood adaptive traits and processes: an overview

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Tansley review
Flood adaptive traits and processes: an overview
Authors for correspondence:
Laurentius A. C. J. Voesenek
Tel: +31 302536849
Email: [email protected]
Laurentius A. C. J. Voesenek1* and Julia Bailey-Serres1,2*
1
Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, the Netherlands; 2Center for Plant Cell
Biology, Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA
Julia Bailey-Serres
Tel: +1 951 827 3738
Email: [email protected]
Received: 25 August 2014
Accepted: 30 October 2014
Contents
Summary
57
I.
Introduction
58
II.
Root acclimations that promote root aeration
60
III.
Regulating reaeration by active emergence in Rumex palustris
and Oryza sativa
62
IV. Limiting O2 starvation with gas films and underwater
photosynthesis
64
V.
Key metabolic acclimations to flooding and low-O2 stress
and their control
65
VI. Managing quiescence of growth during submergence
67
VII. After the deluge
68
VIII. Perspective
69
Acknowledgements
69
References
69
Summary
New Phytologist (2015) 206: 57–73
doi: 10.1111/nph.13209
Key words: adventitious roots, aerenchyma,
ethylene, flooding physiology, hypoxia, radial
oxygen loss, submergence, waterlogging.
Unanticipated flooding challenges plant growth and fitness in natural and agricultural
ecosystems. Here we describe mechanisms of developmental plasticity and metabolic
modulation that underpin adaptive traits and acclimation responses to waterlogging of root
systems and submergence of aerial tissues. This includes insights into processes that enhance
ventilation of submerged organs. At the intersection between metabolism and growth,
submergence survival strategies have evolved involving an ethylene-driven and gibberellinenhanced module that regulates growth of submerged organs. Opposing regulation of this
pathway is facilitated by a subgroup of ethylene-response transcription factors (ERFs), which
include members that require low O2 or low nitric oxide (NO) conditions for their stabilization.
These transcription factors control genes encoding enzymes required for anaerobic metabolism
as well as proteins that fine-tune their function in transcription and turnover. Other mechanisms
that control metabolism and growth at seed, seedling and mature stages under flooding
conditions are reviewed, as well as findings demonstrating that true endurance of submergence
includes an ability to restore growth following the deluge. Finally, we highlight molecular insights
obtained from natural variation of domesticated and wild species that occupy different
hydrological niches, emphasizing the value of understanding natural flooding survival strategies
in efforts to stabilize crop yields in flood-prone environments.
*These authors contributed equally to this work.
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New Phytologist (2015) 206: 57–73 57
www.newphytologist.com
58 Review
New
Phytologist
Tansley review
(a)
(b)
(c)
(d)
Fig. 1 Predicted change in flooding frequency in the 21st Century assuming
increased mean temperature based on projected limited mitigation of CO2
emissions in the representative concentration pathway (RCP) 8.5 scenario
(reprinted with permission from Nature Climate Change (Hirabayashi et al.,
2013), copyright 2013). The color scale indicates the consistency of
projections with the 11 atmosphere–ocean general circulation models
(AOGCMs). For example, regions with greater frequency of floods predicted
by all models are shown in dark blue and lower frequency of floods in dark red.
I. Introduction
Excess of water or floods can negatively impact agricultural yields
by delaying planting, reducing vigor, altering development and
increasing susceptibility to diseases. The financial impact of floods
on agriculture is difficult to calculate, but insurance payouts to
farmers in the USA for flooding damage averaged $24 billion ($US)
yr 1 between 2001 and 2011 (Bailey-Serres et al., 2012a).
Inundation events also effect the distribution and diversity of
species in natural ecosystems (Silvertown et al., 1999). It is expected
that flooding frequency will rise in Southeast Asia, southern India,
East Africa, Siberia and northern parts of South America this
century (IPCC, 2012; Hirabayashi et al., 2013; Fig. 1).
Plants successfully occupy habitats with a wide spectrum of
flooding regimes (i.e. continual, seasonal, ephemeral, shallow,
deep). The remarkable variation in flooding tolerance and adaptive
traits is exemplified by the unequal distribution of species in floodprone Rhine River ecosystems (Vervuren et al., 2003; Van Eck
et al., 2004; Voesenek et al., 2004; van Eck et al., 2006) and species
of major tropical river floodplains such as the Amazon basin
(Parolin et al., 2004; Herrera, 2013) (Fig. 2). Naturally evolved
flooding survival strategies of wild Oryza species are displayed in
some domesticated rice (Oryza sativa) cultivars, particularly those
capable of underwater elongating in deepwater paddies or tolerant
of short-term complete submergence.
During floods, plants endure environmental perturbations such
as a restricted access to atmospheric O2 and CO2, hampered
outward diffusion of plant evolved ethylene (C2H4) (Voesenek &
Sasidharan, 2013), electrochemical soil changes resulting in higher
concentrations of toxic elements including manganese (Mn2+),
iron (Fe2+) and sulfide (H2S, HS , S2 ) (Bailey-Serres &
Voesenek, 2008; Lamers et al., 2012; Zeng et al., 2012) and
reduction in available light (Vervuren et al., 2003). As a consequence, cells and tissues are exposed to pronounced internal
variations in O2 and CO2, and elevation in ethylene as well as
reactive nitrogen and reactive oxygen species (ROS). ROS are
produced at the onset of flooding-induced O2 deprivation as a
New Phytologist (2015) 206: 57–73
www.newphytologist.com
Fig. 2 Examples of plants or vegetation showing survival strategies upon
flooding of the upper Amazon basin of Peru. (a) Aerial prop roots of a Ficus
~o
n River tributary; photographer
ssp. during the low water season (Maran
Julia Bailey-Serres (J.B-S.)). (b) Vigorous regrowth of dormant vegetation
~o;
after desubmergence; an endurance strategy (Ucayali River Supay Can
photographer J.B-S.). The triangle indicates the gradient of regrowth from
first to last desubmerged branches. (c) Elongated petiole and floral stem of
~o
n
common water hyacinth (Eichornia crassipes); an escape strategy (Maran
River tributary; photographer Nicholas Serres). (d) Internode elongation of
Poaceae; an escape strategy (Ucayali River; photographer J. B-S.).
consequence of the inhibition of mitochondrial electron transport
and generation of superoxide that is converted to hydrogen
peroxide by dismutation (Santosa et al., 2007). Increases in
superoxide and hydrogen peroxide are prevalent upon reaeration
(Blokhina & Fagerstedt, 2010; Steffens et al., 2013; Fig. 3).
Although flooding is a compound stress, most research has
focused on the induced energy and carbohydrate crisis caused by
hampered oxidative phosphorylation and low rates of photosynthesis, respectively. Flood-tolerant plants are characterized by a
continuum of survival strategies of which the low-O2 escape
syndrome (LOES) and low-O2 quiescence syndrome (LOQS) are
extremes (reviewed by Bailey-Serres & Voesenek, 2008, 2010;
Voesenek & Bailey-Serres, 2013) (Fig. 3). During escape, various
induced and/or constitutive traits interact in such a way that the
rates of gas exchange between cells and the atmosphere above the
water level increase. Escape phenotypes, not necessarily all present
in one species, include upward bending of leaves (hyponasty),
enhanced shoot elongation, formation of interconnected air-filled
voids (aerenchyma), induction of barriers to radial O2 loss (ROL)
in roots, development of adventitious roots (ARs), formation of gas
films on leaf surfaces, modifications of leaf anatomy and pressurized
gas flow through porous tissues (Jackson & Armstrong, 1999;
Colmer, 2003a; Mommer & Visser, 2005; Colmer & Pedersen,
2007; Polko et al., 2011; Sauter, 2013). Of these traits, there is
growing understanding of the developmental plasticity that drives
aerenchyma and AR formation and elongation of aerial organs. All
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New
Phytologist
Tansley review
(a)
Waterlogging
Hypodermal
RCN1/OsABCG5
Hypodermal
Suberization
Epidermis
Hypodermis
Sclerenchyma
ROL barrier
Cortical
Parenchyma
Ethylene
DPI
(b)
CP
Review 61
RBOH
ROS
Endodermis
Cortical
Aerenchyma
PCD
Ca2+
Stele
METALLOTHIONEIN 2b
SOD
Endoglucanase
Polygalacturonase
Enhanced
aeration
(c)
Epidermal
Degeneration
Submergence
Ethylene
RBOH
Ca2+
DPI
ROS
Ethylene
PCD
above root
SAM
Growth
force
METALLOTHIONEIN 2b
Root
emergence
Adventitious
Root
Primordium
Fig. 4 Three examples of developmental plasticity associated with roots that are promoted when rice is flooded. (a) A radial O2 loss (ROL) barrier and cortical
aerenchyma form as a result of waterlogging to enhance the aeration of root meristems. The ROL is a consequence of deposition of lamellae of suberin between
epidermal and hypodermal cells; it can also include lignification of the sclerenchyma cells. Hypodermal cells that are suberized are referred to as the exodermis.
ROL formation involves up-regulation of genes, including a hypodermal cell ATP-binding cassette (ABC) transporter (REDUCED CULM NUMBER1 (RCN1)/
OsABCG5). (b) Aerenchyma forms as a consequence of programmed cell death (PCD) of cortical parenchyma (CP) cells. This ethylene-promoted process
involves calcium (Ca2+) flux, respiratory burst oxidases (RBOHs), and generation of reactive O2 species (ROS). The process is inhibited by diphenylene iodonium
(DPI), which inhibits RBOHs and other NADPH oxidases. The image was provided by Germain Pauluzzi. SOD, superoxide dismutase. (c) The emergence of
preformed adventitious roots from submerged stem nodes is also mediated by ethylene and blocked by DPI. This developmental response involves localized
epidermal cell degeneration that is driven by the localized force of the emerging root meristem. Processes in the nascent root and subtending epidermal cells are
shown. SAM, shoot apical meristem. The micrograph is from Steffens et al. (2012) with permission (www.plantcell.org; © American Society of Plant Biologists).
The barrier is typically comprised of suberized lamaellae that form
in the exodermal/hypodermal space, particularly near to the root
tip, and lignified schlerenchyma/epidermal cells. These constitute
an efficient ROL barrier as well as an apoplastic blockade between
living cells and the anaerobic and sometimes toxic soil environment
(i.e. saline or highly reduced) (Armstrong et al., 2000; Shiono et al.,
2011; Watanabe et al., 2013). These modifications are also
correlated with minimizing ROL in other waterlogging-tolerant
plants such as wild Zea nicaraguensis (Abiko et al., 2012).
Metabolite profiling of longitudinal sections of ARs of rice
(O. sativa) growing under barrier-forming stagnant conditions
revealed that malic acid and very long chain fatty acids accumulated. The concentrations increased from the root apex to the base,
thus paralleling the development of the barrier (Kulichikhin et al.,
2014). Malic acid is a substrate for fatty acid biosynthesis and thus a
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
precursor for suberin formation. Molecular investigation of the
short and shallow root phenotype of waterlogged reduced culm
number1 (rcn1) mutants of rice led to the recognition of an ATPbinding cassette (ABC) transporter (RCN1/OsABCG5) proposed
to export the very long chain fatty acids and/or their derivatives
across the hypodermal plasma membrane into the apoplast where
they serve as major components of suberin (Shiono et al., 2014)
(Fig. 4a). In comparison to the wild type, rcn1-2 roots fail to
develop effective suberized lamellae or a ROL barrier under
deoxygenated conditions. Elevated ethylene, high CO2 or low O2 is
not essential for barrier formation, but root exudates or cellular
degradation products may be important (Colmer et al., 2006;
Garthwaite et al., 2008).
In addition to increased porosity and a radial diffusion barrier,
many species develop ARs from the hypocotyl or basal stem region
New Phytologist (2015) 206: 57–73
www.newphytologist.com
62 Review
New
Phytologist
Tansley review
when waterlogged (Visser & Voesenek, 2005; Sauter, 2013). These
can replace an existing and often deteriorating primary root system.
Flood-induced ARs typically have higher porosities than the
primary root system (Laan et al., 1989) or ARs that form under
well-aerated conditions (Visser et al., 2000). ARs typically grow in
the better aerated topsoil layers during waterlogging or float in
flood waters (Dawood et al., 2014). The capacity of some ARs to
develop chloroplasts can provide an additional source of O2 and
carbohydrates (Rich et al., 2008, 2012a).
At the cellular level, ethylene and auxin are often integral to
flooding-induced AR formation (reviewed in Visser & Voesenek,
2005). However, in the case of flood-induced ARs from preexisting primordia of rice stem nodes, it is ethylene and not auxin
that signals activation of the cell cycle (Lorbiecke & Sauter, 1999),
which is followed by formation of ROS as measured with electron
paramagnetic resonance spectroscopy (Steffens et al., 2013)
(Fig. 4c). As observed for aerenchyma, this developmental process
also involves the DPI-inhibited plasma membrane RBOHs
(Steffens et al., 2012). The emergence of the delicate AR primordia
involves PCD of the overlying epidermal cells, which is mediated
by ethylene-promoted ROS production. This PCD occurs in a
remarkably spatially specific manner, its location being determined
by the force exerted by the outgrowing meristems. The epidermal
weakening can be elicited by application of ethylene along with the
local force, indicating that a mechanical signal provides the
necessary spatial resolution (Steffens et al., 2012). The reductions
in the METALLOTHIONEIN 2b mRNA also participate in nodal
AR emergence, as a mutant of this ROS ameliorating protein
showed enhanced force-induced epidermal PCD.
III. Regulating reaeration by active emergence in
Rumex palustris and Oryza sativa
Internal aeration of roots via diffusion can take place in completely
submerged plants with the O2 arising from underwater photosynthesis in shoot mesophyll or AR cortical cells or the influx of O2
(a)
from the water layer into the shoot. However, shoot to root aeration
is far more efficient when shoots emerge above the floodwater (Rich
et al., 2012b; Herzog & Pedersen, 2014). For this reason, some
plants from flood-prone environments have evolved the ability to
elongate their porous shoots when underwater to facilitate a LOES.
Because of the carbon costs involved, this trait is restricted to species
or accessions/landraces from environments characterized by shallow, but relatively prolonged floods (Groeneveld & Voesenek,
2003; Voesenek et al., 2004). In species examined to date, a
hormonal hierarchy involving ethylene as a trigger, ABA as a
repressor and GA/auxin as promoters is associated with modulation of underwater elongation growth (Figs 5, 6). Both in rice
accessions from Asia and Rumex species from Rhine floodplains,
differential regulation of this hierarchy is associated with a LOES
and LOQS.
In the case of rice, accessions vary in the degree of underwater
elongation of submerged stems and leaves. The LOES of ‘deepwater’ rice varieties is determined in large part by the SNORKEL
(SK) locus, which encodes the two ERF-VII TFs SK1 and SK2
(Hattori et al., 2009) (Fig. 6a). The ethylene-triggered induction of
SK1/2 during submergence promotes underwater growth of
internodes, enabling plants to elongate underwater at a rate of
25 cm d 1 and to heights of several meters. Two additional
uncharacterized loci on chromosomes 1 and 3 are needed along
with SK1/2 for the full deepwater escape response. Recent
comparison of near-isogenic lines (NILs) differing in the presence
versus absence of the three deepwater quantitative trait loci (QTLs)
(NIL1 + NIL3 + SK1/SK2) revealed that these loci control the
up-regulation of mRNA encoding a rate-limiting GA20 oxidase
(GA20ox), which correlates with increased concentrations of
bioactive GA1 and GA4 in internode tissue, although the
contributions of the individual loci remain unclear (Ayano et al.,
2014). Mutation of GA3ox, which acts after GA20ox, or disruption
of genes required for GA responsiveness (i.e. the genes encoding the
GA receptor Gibberellin-insensitive dwarf (GID) and proteins
involved in its turnover) significantly limited underwater
(b)
Fig. 5 Factors controlling underwater petiole elongation in Rumex palustris. (a) Time-scale of modulation of genes, hormones and cellular factors associated
with promotion of petiole elongation in submerged plants. Pathways in the shaded region in green are abscisic acid (ABA) dependent. (b) Photograph following
7 d of submergence. Data are based on van Veen et al. (2013). NCED, 9-CIS-EPOXYCAROTENOID DIOXYGENASE; ABA8ox, ABA-8-HYDROXYLASE; HDZIPII, CLASS II HOMEODOMAIN-LEUCINE-ZIPPER; COP1, CONSTITUTIVE PHOTOMORPHOGENIC1; EXPs, EXPANSINs; GA3ox, GA3 OXIDASE; GA1,
gibberellin1; IAA, indole-3-acetic acid; PIF, PHYTOCHROME INTERACTING FACTORS; XTHs, XYLOGLUCANENDOTRANSGLUCOSYLASE-HYDROLASEs.
New Phytologist (2015) 206: 57–73
www.newphytologist.com
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New
Phytologist
Tansley review
(a)
Waterlogging
Hypodermal
RCN1/OsABCG5
Hypodermal
Suberization
Epidermis
Hypodermis
Sclerenchyma
ROL barrier
Cortical
Parenchyma
Ethylene
DPI
(b)
CP
Review 61
RBOH
ROS
Endodermis
Cortical
Aerenchyma
PCD
Ca2+
Stele
METALLOTHIONEIN 2b
SOD
Endoglucanase
Polygalacturonase
Enhanced
aeration
(c)
Epidermal
Degeneration
Submergence
Ethylene
RBOH
Ca2+
DPI
ROS
Ethylene
PCD
above root
SAM
Growth
force
METALLOTHIONEIN 2b
Root
emergence
Adventitious
Root
Primordium
Fig. 4 Three examples of developmental plasticity associated with roots that are promoted when rice is flooded. (a) A radial O2 loss (ROL) barrier and cortical
aerenchyma form as a result of waterlogging to enhance the aeration of root meristems. The ROL is a consequence of deposition of lamellae of suberin between
epidermal and hypodermal cells; it can also include lignification of the sclerenchyma cells. Hypodermal cells that are suberized are referred to as the exodermis.
ROL formation involves up-regulation of genes, including a hypodermal cell ATP-binding cassette (ABC) transporter (REDUCED CULM NUMBER1 (RCN1)/
OsABCG5). (b) Aerenchyma forms as a consequence of programmed cell death (PCD) of cortical parenchyma (CP) cells. This ethylene-promoted process
involves calcium (Ca2+) flux, respiratory burst oxidases (RBOHs), and generation of reactive O2 species (ROS). The process is inhibited by diphenylene iodonium
(DPI), which inhibits RBOHs and other NADPH oxidases. The image was provided by Germain Pauluzzi. SOD, superoxide dismutase. (c) The emergence of
preformed adventitious roots from submerged stem nodes is also mediated by ethylene and blocked by DPI. This developmental response involves localized
epidermal cell degeneration that is driven by the localized force of the emerging root meristem. Processes in the nascent root and subtending epidermal cells are
shown. SAM, shoot apical meristem. The micrograph is from Steffens et al. (2012) with permission (www.plantcell.org; © American Society of Plant Biologists).
The barrier is typically comprised of suberized lamaellae that form
in the exodermal/hypodermal space, particularly near to the root
tip, and lignified schlerenchyma/epidermal cells. These constitute
an efficient ROL barrier as well as an apoplastic blockade between
living cells and the anaerobic and sometimes toxic soil environment
(i.e. saline or highly reduced) (Armstrong et al., 2000; Shiono et al.,
2011; Watanabe et al., 2013). These modifications are also
correlated with minimizing ROL in other waterlogging-tolerant
plants such as wild Zea nicaraguensis (Abiko et al., 2012).
Metabolite profiling of longitudinal sections of ARs of rice
(O. sativa) growing under barrier-forming stagnant conditions
revealed that malic acid and very long chain fatty acids accumulated. The concentrations increased from the root apex to the base,
thus paralleling the development of the barrier (Kulichikhin et al.,
2014). Malic acid is a substrate for fatty acid biosynthesis and thus a
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
precursor for suberin formation. Molecular investigation of the
short and shallow root phenotype of waterlogged reduced culm
number1 (rcn1) mutants of rice led to the recognition of an ATPbinding cassette (ABC) transporter (RCN1/OsABCG5) proposed
to export the very long chain fatty acids and/or their derivatives
across the hypodermal plasma membrane into the apoplast where
they serve as major components of suberin (Shiono et al., 2014)
(Fig. 4a). In comparison to the wild type, rcn1-2 roots fail to
develop effective suberized lamellae or a ROL barrier under
deoxygenated conditions. Elevated ethylene, high CO2 or low O2 is
not essential for barrier formation, but root exudates or cellular
degradation products may be important (Colmer et al., 2006;
Garthwaite et al., 2008).
In addition to increased porosity and a radial diffusion barrier,
many species develop ARs from the hypocotyl or basal stem region
New Phytologist (2015) 206: 57–73
www.newphytologist.com
62 Review
New
Phytologist
Tansley review
when waterlogged (Visser & Voesenek, 2005; Sauter, 2013). These
can replace an existing and often deteriorating primary root system.
Flood-induced ARs typically have higher porosities than the
primary root system (Laan et al., 1989) or ARs that form under
well-aerated conditions (Visser et al., 2000). ARs typically grow in
the better aerated topsoil layers during waterlogging or float in
flood waters (Dawood et al., 2014). The capacity of some ARs to
develop chloroplasts can provide an additional source of O2 and
carbohydrates (Rich et al., 2008, 2012a).
At the cellular level, ethylene and auxin are often integral to
flooding-induced AR formation (reviewed in Visser & Voesenek,
2005). However, in the case of flood-induced ARs from preexisting primordia of rice stem nodes, it is ethylene and not auxin
that signals activation of the cell cycle (Lorbiecke & Sauter, 1999),
which is followed by formation of ROS as measured with electron
paramagnetic resonance spectroscopy (Steffens et al., 2013)
(Fig. 4c). As observed for aerenchyma, this developmental process
also involves the DPI-inhibited plasma membrane RBOHs
(Steffens et al., 2012). The emergence of the delicate AR primordia
involves PCD of the overlying epidermal cells, which is mediated
by ethylene-promoted ROS production. This PCD occurs in a
remarkably spatially specific manner, its location being determined
by the force exerted by the outgrowing meristems. The epidermal
weakening can be elicited by application of ethylene along with the
local force, indicating that a mechanical signal provides the
necessary spatial resolution (Steffens et al., 2012). The reductions
in the METALLOTHIONEIN 2b mRNA also participate in nodal
AR emergence, as a mutant of this ROS ameliorating protein
showed enhanced force-induced epidermal PCD.
III. Regulating reaeration by active emergence in
Rumex palustris and Oryza sativa
Internal aeration of roots via diffusion can take place in completely
submerged plants with the O2 arising from underwater photosynthesis in shoot mesophyll or AR cortical cells or the influx of O2
(a)
from the water layer into the shoot. However, shoot to root aeration
is far more efficient when shoots emerge above the floodwater (Rich
et al., 2012b; Herzog & Pedersen, 2014). For this reason, some
plants from flood-prone environments have evolved the ability to
elongate their porous shoots when underwater to facilitate a LOES.
Because of the carbon costs involved, this trait is restricted to species
or accessions/landraces from environments characterized by shallow, but relatively prolonged floods (Groeneveld & Voesenek,
2003; Voesenek et al., 2004). In species examined to date, a
hormonal hierarchy involving ethylene as a trigger, ABA as a
repressor and GA/auxin as promoters is associated with modulation of underwater elongation growth (Figs 5, 6). Both in rice
accessions from Asia and Rumex species from Rhine floodplains,
differential regulation of this hierarchy is associated with a LOES
and LOQS.
In the case of rice, accessions vary in the degree of underwater
elongation of submerged stems and leaves. The LOES of ‘deepwater’ rice varieties is determined in large part by the SNORKEL
(SK) locus, which encodes the two ERF-VII TFs SK1 and SK2
(Hattori et al., 2009) (Fig. 6a). The ethylene-triggered induction of
SK1/2 during submergence promotes underwater growth of
internodes, enabling plants to elongate underwater at a rate of
25 cm d 1 and to heights of several meters. Two additional
uncharacterized loci on chromosomes 1 and 3 are needed along
with SK1/2 for the full deepwater escape response. Recent
comparison of near-isogenic lines (NILs) differing in the presence
versus absence of the three deepwater quantitative trait loci (QTLs)
(NIL1 + NIL3 + SK1/SK2) revealed that these loci control the
up-regulation of mRNA encoding a rate-limiting GA20 oxidase
(GA20ox), which correlates with increased concentrations of
bioactive GA1 and GA4 in internode tissue, although the
contributions of the individual loci remain unclear (Ayano et al.,
2014). Mutation of GA3ox, which acts after GA20ox, or disruption
of genes required for GA responsiveness (i.e. the genes encoding the
GA receptor Gibberellin-insensitive dwarf (GID) and proteins
involved in its turnover) significantly limited underwater
(b)
Fig. 5 Factors controlling underwater petiole elongation in Rumex palustris. (a) Time-scale of modulation of genes, hormones and cellular factors associated
with promotion of petiole elongation in submerged plants. Pathways in the shaded region in green are abscisic acid (ABA) dependent. (b) Photograph following
7 d of submergence. Data are based on van Veen et al. (2013). NCED, 9-CIS-EPOXYCAROTENOID DIOXYGENASE; ABA8ox, ABA-8-HYDROXYLASE; HDZIPII, CLASS II HOMEODOMAIN-LEUCINE-ZIPPER; COP1, CONSTITUTIVE PHOTOMORPHOGENIC1; EXPs, EXPANSINs; GA3ox, GA3 OXIDASE; GA1,
gibberellin1; IAA, indole-3-acetic acid; PIF, PHYTOCHROME INTERACTING FACTORS; XTHs, XYLOGLUCANENDOTRANSGLUCOSYLASE-HYDROLASEs.
New Phytologist (2015) 206: 57–73
www.newphytologist.com
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New
Phytologist
Tansley review
(a)
Review 63
(b)
Fig. 6 Factors controlling underwater shoot and internode elongation promoted by submergence and modulated by loci present in some accessions of rice
(Oryza sativa). The submergence tolerance gene SUBMERGENCE1A (SUB1A) was identified in a landrace grown in flood-prone lowlands of eastern India (Xu
et al., 2006). Three quantitative trait loci are responsible for underwater elongation in deepwater rice: SNORKEL1 and 2 (SK1/2) and two uncharacterized loci
on chromosomes 1 and 3 (QTL 1 & 3) (Hattori et al., 2009; Ayano et al., 2014). ETHYLENE INSENSITIVE 3 (EIN3) binds the SK promoters to drive ethyleneinduced transcription. (a) Model illustrating the genes and hormones associated with promotion or repression of elongation growth in submerged rice. SUB1A
and SK1/2 are key regulators. SUB1A limits elongation growth whereas SK1/2 promote elongation of underwater internodes 6 and above. All three are
ethylene-responsive TFs of the subfamily group VII. Changes in levels of ethylene, cellular energy and O2 are signals that regulate responses in submerged
tissues. Abscisic acid (ABA), gibberellins (GAs) and brassinosteroids (BRs) are important. SUB1A limits elongation through multiple mechanisms including
increased accumulation of the GA-response transcriptional inhibitors SLENDER RICE 1 (SLR1) and SLENDER RICE-LIKE 1 (SLRL1), inhibition of ethylene
biosynthesis, and restriction of chlorophyll degradation, probably mediated by methyl-jasmonate (Fukao et al., 2012). ABA8ox, abscisic acid 8-hydroxylase;
Chl. deg., chlorophyll degradation; C, carbon; N, nitrogen; ROS, reactive oxygen species; SUB1C, SUBMERGENCE1C; CIPK15, CALCINEURIN B-LIKE
INTERACTING BINDING KINASE15; SUS, SUCROSE SYNTHASE; ADH1, ALCOHOL DEHYDROGENASE1; PDC1, PYRUVATE DECARBOXYLASE1; AlaAT,
ALANINE AMINOTRANSFERASE; EXPs, EXPANSINs. (b) Photograph of shoots of IR64 rice elongating underwater, a variety that lacks SUB1A or SK1/2.
elongation when introduced into the genotype with the three
deepwater QTL (NIL1 + NIL2 + SK1/SK2). Nondeepwater rice
varieties, such as those widely grown since the Green Revolution of
the 1960s, carry the defective semidwarf1 (sd1) allele of GA20ox on
chromosome 1, which confers reduced GA biosynthesis. It is
probably the absence of SK1/SK2 and possibly differences in genes/
alleles at QTLs on chromosomes 1 and 3 that are responsible for the
partial LOES characteristic of modern rice cultivars. As will be
discussed futher in Section VI, the SUB1A gene of the
SUBMERGENCE1 (SUB1) locus confers LOQS and fits into the
same regulatory module as SK1/2 but conversely restricts GAdriven starch catabolism and shoot elongation growth, conferring
tolerance to submergence (Fig. 6).
The LOQS and LOES of both rice and the dicot R. palustris
involve the conserved molecular triumvirate that includes ethylene,
ABA and GA. As compared with the internodal elongation of
deepwater rice, LOES is manifested as underwater elongation of
petioles of R. palustris. Contrastingly, petioles of the related
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Rumex acetosa, a species from rarely flood riparian sites, show a
reduced elongation rate when submerged. This is caused by an
inability to reduce ABA concentrations, which appears to be a
prerequisite for underwater elongation growth (Benschop et al.,
2005; van Veen et al., 2013). Interestingly, in R. palustris, variation
between ecotypes in submergence-induced petiole elongation
occurs at the level of ethylene-controlled down-regulation of ABA.
In R. palustris ecotypes that rapidly elongate, submerged petioles
display stronger submergence-induced declines in ABA content
than slowly elongating ecotypes (Chen et al., 2010).
Fig. 5 presents the current understanding of the petiole elongation in R. palustris upon complete submergence. The commencement of underwater elongation is preceded by cellular
accumulation of ethylene, which continues to be synthesized but
has hampered diffusion out of tissues because of the surrounding
floodwater (Bailey-Serres & Voesenek, 2008). The increase in
endogenous ethylene content is detected within 1 h but probably
occurs much faster, as ethylene-dependent acidification of the
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apoplast is detected within 10 min (Vreeburg et al., 2005). This
reduction in apoplastic pH is optimal for the activity of cell wallloosening proteins (Kende et al., 2004). Elevated ethylene also
stimulates, within 2 h of submergence, the abundance of mRNAs
encoding cell wall-modifying proteins such as expansins (EXP) and
xyloglucanendotransglucosylase-hydrolases (XTH). This is concomitant with a reduction in mRNAs encoding 9-cis-epoxycarotenoid dioxygenase (NCED), which catalyzes the rate-limiting step
in ABA biosynthesis (Benschop et al., 2005; Vreeburg et al., 2005;
van Veen et al., 2013). Analyses of petiole transcripts, using global
mRNA-seq and targeted transcript analyses, further refined the
understanding of this hierarchical response (van Veen et al., 2013).
mRNAs encoding ABA-8-hydroxylase, which converts ABA to
inactive phaseic acid, are induced as early as 1 h after submergence
(H. van Veen, pers. comm.). Finally, PHYTOCHROME
INTERACTING FACTORS (PIF) mRNAs are up-regulated
within 2–3 h.
Indications that auxin also plays a role, specifically in the early
hours of submergence-induced petiole elongation, come from
experiments on R. palustris in which the endogenous indole-3acetic acid (IAA) concentration in petioles was lowered by leaf blade
removal (Cox et al., 2004). This treatment prolonged the lag-phase
before petiole elongation from 2 to 8 h, an effect that could be
rescued completely by addition of the IAA analog 1-naphthaleneacetic acid (NAA) (Cox et al., 2006). Consistent with a role for
auxin is the increase of the endogenous IAA concentration in both
adaxial and abaxial epidermal petiole slices within 2 h of submergence (Cox et al., 2004) and the up-regulation of several AUX/IAA
genes in the petioles of R. palustris but not R. acetosa (van Veen
et al., 2013). Interestingly, auxin is necessary to regulate several
XTHs in A. thaliana during shade-induced growth responses, a
response that is phenotypically very similar to underwater petiole
elongation (Pierik et al., 2010; Keuskamp et al., 2011).
The role of ABA in regulation of petiole growth is also evident
from the observation that ABA concentrations declined by 80%
within 1 h of submergence. This response seems to be a general
reaction in Rumex as it was observed in all petioles, leaf blades and
roots. The strong reduction of petiole elongation in submerged
plants that received exogenous ABA demonstrates the importance
of ABA-dependent regulation (Benschop et al., 2005, 2006). After
3 h of submergence, the GA biosynthesis gene GA3ox and a set of
genes known from photomorphogenic and shade avoidance
responses (KIDARI, CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1) and CLASS II HOMEODOMAIN-LEUCINEZIPPER (HD-ZIPII)) were up-regulated (van Veen et al., 2013).
The first increase in bioactive GA1 was observed after 4–5 h, too late
to explain the initiation of underwater growth. This suggests that
the initial elongation growth in R. palustris petioles operates
independently of GA (Benschop et al., 2006). The increase in the
expression of typical shade avoidance-associated genes suggests a
role for phytochrome-dependent signaling during underwater
elongation. However, the decrease in the red : far red ratio (R : FR)
from 2.2 to 1.6 that occurs during submergence was not sufficient
to induce elongation and/or expression of photomorphogenesis
genes under nonsubmerged conditions. Moreover, artificially
filtering of FR wavelengths, resulting in higher R : FR ratios
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underwater, did not reduce the elongation response. These data
strongly suggest that the light signaling machinery is activated in
submerged plants, independent of phytochrome signaling (van
Veen et al., 2013). Both KIDARI and COP1 interact with LONG
HYPOCOTYL IN FAR-RED1 (HFR1). This basic helix-loophelix TF forms heterodimers with PIFs, thus preventing their
activation of target genes associated with enhanced shoot elongation (Galstyan et al., 2011). COP1 functions as an E3 ligase and
targets, among other proteins, HFR1 for degradation (Yang et al.,
2005). The heterodimerization of KIDARI with HFR1 releases
PIFs from inhibition (Hyun & Lee, 2006). We surmise that
promotion of ethylene-regulated transcription of PIFs in combination with the increase of both KIDARI and COP1 elevates
concentrations of activated PIFs, leading to stimulation of growthrelated processes (van Veen et al., 2013).
Underwater shoot elongation has been studied in depth in two
model plants: R. palustris and O. sativa. The conserved interaction
between the hormones ethylene, ABA and GA perceives
submergence and regulates the upsurge of cell expansion in both
species. ERF-VII TFs regulate underwater growth in rice, whereas
light-signaling genes regulate enhance shoot elongation in
R. palustris. The latter observation demonstrates the downstream
similarity of growth control during shade avoidance and
underwater elongation.
IV. Limiting O2 starvation with gas films and
underwater photosynthesis
Submerged leaves develop diffusive boundary layers with a
thickness very similar to that of leaves in air. However, the 104fold lower diffusion coefficient of gases in water causes a
proportionally lower gas flux at a similar concentration gradient
in the boundary layer of water-surrounded leaves. These boundary
layers contribute a very large proportion of the resistance to CO2
and O2 exchange in submerged leaves, constraining photosynthesis
and respiration (Pedersen et al., 2013). Another limitation for
underwater photosynthesis is the exponential decrease of light with
depth (Colmer et al., 2011). Dissolved organic matter and
suspended particles further attenuate light penetration in floodwaters (Vervuren et al., 2003). Consequently, net photosynthesis of
submerged terrestrial leaves is often significantly reduced compared
with aerial leaves. It is, however, also lower than the rates in leaves of
aquatic plant species because of the general lack of beneficial leaf
traits (Colmer et al., 2011; Herrera, 2013). Nevertheless, in a range
of terrestrial species submergence in the presence of light is
beneficial, highlighting the importance of underwater photosynthesis for submergence survival (Vervuren et al., 2003; Mommer
et al., 2006; Vashisht et al., 2010; Lee et al., 2011; Herrera, 2013).
In some submerged terrestrial plants, new leaves develop that are
characterized by a higher specific leaf area, reoriented chloroplasts
toward the epidermis of the leaf as well as thinner cuticles and cell
walls (Mommer et al., 2005b). Other relevant traits are the
development of dissected leaves under water and the maintenance
of gas films (Colmer et al., 2011). All of these traits reduce diffusion
resistance for CO2 and thus increase the rates of underwater
photosynthesis (Mommer et al., 2005a). Rumex palustris develops
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new leaves under water and acclimations in these leaves (Mommer
et al., 2005b) lead to a 38-fold decrease of the diffusion resistance to
CO2 under water (Mommer et al., 2005a).
Many terrestrial plants have water-repellent or hydrophobic leaf
surfaces that retain a thin layer of air (gas film) when submerged.
This enlarges the gas–water interface and allows fast CO2 diffusion
within the air layer so that stomata can stay open. This was found to
result in a 1.5–6-fold increase in the rate of underwater photosynthesis compared with leaves in which the gas film was removed, in
laboratory and field studies (Colmer et al., 2011; Winkel et al., 2011,
2013, 2014; Pedersen et al., 2013). There is evidence of variation in
this trait in rice, with higher net underwater photosynthesis and
longer leaf gas film retention in the submergence-tolerant landrace
FR13A over a 12-d submergence period in plants grown in the field
(Winkel et al., 2014). Although gas film persistence was correlated
with better maintenance of carbohydrates during submergence in
FR13A, the duration of gas film retention was less in a Sub1 variety
(Swarna-Sub1), indicating that genetic determinants other than
the submergence-tolerant determinant SUB1A contribute to gas
film formation or underwater photosynthesis.
Gas films and the above-mentioned morphological and anatomical leaf acclimations improve not only the inward diffusion of
CO2 in the light, but also the diffusion of O2 from the water layer
into the leaf in turbid waters or at night (Pedersen et al., 2009;
Verboven et al., 2014). A novel function for leaf gas films was
recently described for the annual legume Melilotus siculus
submerged in saline waters. This species has gas films for the first
3 d of submergence on both leaf surfaces that not only improve gas
exchange but also prevent salt intrusion (Teakle et al., 2014).
V. Key metabolic acclimations to flooding and low-O2
stress and their control
Dynamic changes in mRNAs and metabolites in response to
submergence, waterlogging or hypoxia (typically < 10% O2 in
surrounding air or aqueous media) have been evaluated in a wide
range of species including A. thaliana, rice, other crops, deciduous
trees and Chlamydomonas (reviewed by Sweetlove et al., 2010;
Grossman et al., 2011; Narsai et al., 2011; Bailey-Serres et al.,
2012b; Banti et al., 2013; Kreuzwieser & Rennenberg, 2014;
Mustroph et al., 2014; Shingaki-Wells et al., 2014). These surveys
demonstrate both similarities and differences in metabolic acclimations. With near uniformity, environmental conditions with
low O2 elevate mRNAs encoding enzymes of an anaerobic
metabolism module comprised of starch consumption (amylases),
sucrose catabolism (sucrose synthase), glycolysis (phosphofructokinase), and pyruvate metabolism to ethanol (pyruvate decarboxylase (PDC)), alcohol dehydrogenase (ADH) or lactate (lactate
dehydrogenase), as well as alanine (alanine aminotransferase),
GABA (glutamate decarboxylase), succinate, and several glucogenic amino acids. The current hypothesis is that restriction of
mitochondrial electron transport caused by limited O2 availability
is accompanied by a bifurcation of the TCA cycle that enhances
production of ATP by the TCA enzyme succinyl-CoA ligase
(Rocha et al., 2010; Sweetlove et al., 2010; Bailey-Serres et al.,
2012a). This scenario requires further confirmation by metabolic
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flux analyses (Szecowka et al., 2013), which might also consider
how anaerobic metabolism is curtailed and its products consumed
upon reoxygenation or desubmergence (Narsai et al., 2009;
Barding et al., 2012, 2013; Mustroph et al., 2014).
A fundamental advance was made with the recognition in A.
thaliana that transcription of anaerobic metabolism genes is
governed by O2-regulated localization and turnover of the ERFVIIs (Gibbs et al., 2011; Licausi et al., 2011). The underlying O2
homeostasis sensing mechanism involves the arginine branch of the
evolutionarily conserved N-end rule pathway of targeted proteolysis (Arg/N-end rule pathway), which has been summarized in
several reviews (Bailey-Serres & Voesenek, 2010; Banti et al., 2013;
Licausi et al., 2013; Gibbs et al., 2014a). Briefly, there are five ERFVIIs genes in A. thaliana. Three of these are constitutively expressed
(Related to AP2 12 (RAP2.12), RAP2.2 and RAP2.3) and further
up-regulated by darkness or ethylene, and the other two
(HYPOXIA RESPONSIVE ERF1/2) are highly induced at transcriptional and translational levels by O2 deprivation at multiple
developmental stages. ERF-VII turnover by the Arg/N-end rule
pathway occurs when both O2 and nitric oxide (NO) are available,
suggesting that ERF-VIIs participate in homeostatic O2- and NOsensing mechanisms (Gibbs et al., 2011, 2014b; Licausi et al.,
2011). Reduction of O2 by transfer of plants from normoxia to
hypoxia or inhibition of NO accumulation by genetic or chemical
means is sufficient to stabilize these proteins.
The core Arg/N-end pathway that regulates ERF-VII turnover is
relatively well characterized (Fig. 7). The process requires a cysteine
as the second residue of the protein and several enzymes:
methionine aminopeptidase (MetAP), arginyl aminotransferase
(ATE) and the N-recognin E3 ubiquitin-ligase (proteolysis 6
(PRT6)). MetAP-mediated removal of the initiator methionine
yields an N-terminal Cys that is a substrate for oxidation. This may
occur spontaneously, but is catalyzed by the O2-dependent plant
cysteine oxidase (PCO1/2), which oxidizes N-terminal, but not
internal Cys residues (Weits et al., 2014). Work in animals and now
plants suggests that this modification probably requires both O2
and NO (Gibbs et al., 2014a). The presumed resultant NH2-Cyssulfinic or NH2-Cys-sulfonic moiety structurally resembles an Nterminal aspartic acid that is recognized by ATE. This enzyme adds
an N-terminal Arg from a tRNAARG to generate an NH2-Arg-Cysox
terminus. In these three steps, the tertiary destabilizing N-terminal
Cys is converted to the secondary destabilizing N-terminal Cysox
and finally to a primary destabilizing NH2-Arg. The resultant Ndegron is recognized by PRT6, a single-subunit Really Interesting
New Gene (RING)-domain N-recognin coupled with an E2 ligase
that adds ubiquitin to an internal lysine residue of the ERF-VII.
This completes the marking of the protein for 26S proteasomemediated destruction.
A challenging question is what cellular concentration of O2
promotes stabilization and activation of these ERF-VIIs. Kosmacz
et al. (2014) demonstrated that reduction of atmospheric O2 below
10% increases the nuclear localization of RAP2.12. As O2
concentrations decline, RAP2.12 is relocalized from the plasma
membrane to the nucleus, concomitant with increased accumulation of hypoxia-responsive mRNAs. The proportion of cells with
detectable nuclear localized RAP2.12-GFP increases significantly
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Fig. 7 Oxygen (O2) sensing via the arginine branch of the N-end rule regulates positive and negative transcriptional regulation of core hypoxia response genes
in Arabidopsis thaliana. The five group VII ethylene-responsive TFs (ERF-VIIs) of A. thaliana, which include Related to AP2 12 (RAP2.12), are turned over by the
N-end rule pathway of targeted proteolysis (Gibbs et al., 2011; Licausi et al., 2011). This multistep pathway begins with initiator methionine removal by a
Methionine aminopeptidase (MetAP1/2). The new amino-terminus, a cysteine residue, is a target for oxidation to Cys-sulfinic or Cys-sulfonic acid (Cysox), a
reaction promoted by O2 and nitric oxide (NO) generated from nitrate reductases (i.e. NIA1/2) (Gibbs et al., 2014a,b) and possibly other sources. It is proposed
that N-Cysox-RAP2.12 is sequentially modified by Arginyl aminotransferase1/2 (ATE1/2) and a ubiquitin E3 ligase (Proteolysis 6 (PRT6)), triggering
degradation under aerobic conditions (Licausi et al., 2011), whereas the oxidation of the N-Cys is limited when O2 is limited. As O2 concentrations in air decline
below 10% or within 1 h of O2 deprivation, RAP2.12 is stabilized as confirmed by accumulation of RAP2.12-GFP within nuclei (Kosmacz et al., 2014). The red
triangle is representative of the increase in stability as O2 concentrations decline. Nuclear RAP2.12 is associated with increased core hypoxia-responsive gene
transcript levels (Gibbs et al., 2011; Licausi et al., 2011). Directed studies recognize PYRUVATE DECARBOXYLASE1 (PDC1), HYPOXIA RESPONSIVE ERF1/2
(HRE1/2), trihelix TF HYPOXIA RESPONSE ATTENUATOR1 (HRA1), PLANT CYSTEINE OXIDASE1/2 (PCO1/2) and HEMOGLOBIN1 (HB1) as targets of
RAP2.12 transcriptional activation (Giuntoli et al., 2014; Klecker et al., 2014; Weits et al., 2014). HRE2 transcriptionally activates PDC1 (Julia Bailey-Serres,
unpublished). Blue arrows, transcriptional activation. Both HRA1 and PCO1/2 negatively regulate RAP2.12. HRA1 acts by direct interaction, limiting the
transcriptional activation of PDC1 (Giuntoli et al., 2014). Dashed arrow, limited HRA1 activation by RAP2.12 as a result of direct binding of HRA1 to its
promoter. This relationship between HRA1 and RAP2.12 may enable a pulse of PDC1 transcription. PCO1/2 inhibit RAP2.12 by catalyzing its N-Cys oxidation
to initiate RAP2.12 turnover. The gray box highlights proposed regulation by NO, whereby HB1 contributes to the fine-tuning of RAP2.12 accumulation by
scavenging NO produced by NIA1/2 or mitochondria during O2 deprivation. Arg, arginine.
within 3 h of exposure to 1% O2, with a significant decline in
nuclear RAP2.12 with 3 h of reoxygenation (Kosmacz et al., 2014).
The regulation of ERF-VII accumulation and activity is
complex. In addition to the core Arg/N-end rule components
and O2, there is involvement of PCO1/2 and NO. Disruption of
PCO1/2 limits the degradation of RAP2.12 and reduces submergence tolerance of rosette-stage plants (Weits et al., 2014).
Inhibition of NO accumulation by disruption of NITRATE
REDUCTASE1/2 (NIR1/2) or treatment with a chemical NO
scavenger also stabilizes ERF-VIIs (Gibbs et al., 2014b). Interestingly, PCO1/2, NIR1/2 and HEMOGLOBIN1 (HB1), the last
encoding an NO scavenger, are all hypoxia-responsive genes
(Mustroph et al., 2009). Moreover, these genes are constitutively
up-regulated in the prt6-1 mutant, indicating that they are under
Arg/N-end rule pathway control (Gibbs et al., 2011). At least
PCO1/2 and HB1 are under direct ERF-VII regulation (Klecker
et al., 2014; Weits et al., 2014). As mitochondrial production of
NO is elevated under hypoxia and regulated by HB1 (reviewed by
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Bailey-Serres & Voesenek, 2008; Igamberdiev et al., 2010; Hill,
2012), it can be proposed that HB1 contributes to regulation of
ERF-VII accumulation by removal of NO during hypoxia (Fig. 7,
dashed box). The role of HB1 and NO in the regulation of ERF-VII
turnover as O2 concentrations vary deserves further scrutiny.
There is cellular control of RAP2.12 by another RAP2.12regulated and hypoxia-responsive gene. The trihelix TF hypoxia
response attenuator 1 (HRA1) directly binds RAP2.12 and inhibits
its transcriptional activation of PDC1 and other hypoxia-responsive genes (Giuntoli et al., 2014). This negative control occurs
under low-O2 conditions, but is restricted because HRA1 binds its
own promoter and thereby limits its activation by RAP2.12. It is
envisioned that the coupling of RAP2.12 and HRA1 function
allows for pulsing of transcription of genes that promote anaerobic
metabolism.
Other regulatory modules are relevant to low-O2 survival in
A. thaliana and possibly other plants. Another regulatory mode,
limited to shoot tissue, involves the TF PHOSPHATE
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STARVATION RESPONSE1 (PHR1) which is known to activate a
phosphate starvation-response gene network (Klecker et al., 2014).
Under hypoxia, PHR1 drives expression of galactolipid biosynthesis genes associated with modification of the composition of
plastid membranes. It is hypothesized that disturbance of photosynthesis by hypoxia promotes chloroplast-to-nucleus signaling
that triggers the PHR1 network, thereby providing an adaptive
benefit for low-O2 or reoxygenation survival. A second module
influenced by low O2 is the low-energy signaling nexus that
reprograms gene expression at transcriptional and translational
levels, and impacts carbon and nitrogen metabolism, the cell cycle
and development (Baena-Gonzalez et al., 2007; Tome et al., 2014).
Key components of the low-energy network include the conserved
protein kinases sucrose nonfermenting-1-related protein kinase 1
(SnRK1) and target of rapamycin (TOR). The efficient anaerobic
germination of rice seeds involves SnRK1 and an upstream kinase
(reviewed by Lee et al., 2014). Future studies that take advantage of
mutants, inducible RNAi lines and specific inhibitors of key
components of these pathways will clarify their importance in
flooding survival strategies.
VI. Managing quiescence in growth during
submergence
A success story of modern agriculture is the introduction of the
SUB1 locus from the submergence-tolerant landrace FR13A of rice
into popular high-yielding varieties and the rapid adoption of these
‘Sub1’ varieties in flood-prone regions in Asia (Bailey-Serres et al.,
2010; Ismail et al., 2013; Singh et al., 2013). The SUB1 locus
encodes two to three ERF-VII TFs including SUB1A, which
regulates LOQS traits that prolong survival of short but deep
submergence events (Fukao et al., 2006; Xu et al., 2006) as well as
recovery and regrowth following desubmergence (Fukao et al.,
2011). The LOES provided by SK1/SK2 is antithetical to the
LOQS provided by the gene SUB1A-1.
The mechanisms of submergence tolerance determined by
SUB1A-1 have been intensively studied with a pair of NILs
differing only in the region of chromosome 9 comprising the SUB1
locus and transgenics that ectopically express SUB1A-1. These have
revealed that SUB1A plays multiple roles during submergence and
the desubmergence recovery period in shoot tissues. Its role during
submergence centers on the same hormone triumvirate that
regulates elongation growth in R. palustris and deepwater rice
(Fig. 6).
As seen for SK1/2, submergence rapidly up-regulates SUB1A-1
transcripts by over 200-fold (Fukao et al., 2006). This is probably a
response to the rapid entrapment of ethylene in submerged tissues.
Factors such as low O2 or low energy may also promote SUB1A
transcript abundance during submergence, as the maximal induction by ethylene is far below that observed under submergence. As
observed for deepwater rice, submergence promotes ethylene
biosynthesis in lowland varieties, but this is significantly curbed in
SUB1A-1 genotypes (Fukao et al., 2006). The increase in ethylene
is associated with a decline in ABA content whether or not SUB1A1 is present (Fukao & Bailey-Serres, 2008). However, unlike
deepwater rice which biosynthesizes GA in submerged tissue
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(Hattori et al., 2009; Ayano et al., 2014), lowland rice shoots
display little or no increase in GA4 (Schmitz et al., 2013). The
limited GA biosynthesis in these lowland varieties during submergence may relate to the presence of the loss-of-function sd-1 allele
(OsGA20ox2). The deepwater elongating varieties C9285 and
NIL1 + NIL3 + SK1/SK2, by contrast, possess a functional and
submergence-induced OsGAox2 allele that may be essential for
their c. 8-fold increase in GA1 and GA4 (Ayano et al., 2014).
In rice, GA4 binds its receptor GID to promote its interaction
with the DELLA domain-containing GRAS TF Slender rice1
(SLR1) which is bound to GA-responsive genes to limit their
transcription. This stimulates ubiquitylation of SLR1 by SCFSLY1/
GID2
, a Skp1-Cullin-F box protein (SCF) E3 ligase that includes the
F-box protein Gibberellin insensitive dwarf 2 (GID2) (Hauvermale et al., 2012). Ubiquitylation of SLR1 targets it for proteasome
degradation, freeing GID1 for reuse and enabling the transcriptional activation of the genes that had been SLR1 bound. In this
manner, GA4 can promote the activation of genes associated with
elongation growth. However, rice possesses a second GRAS
domain protein, Slender rice1-like1 (SLRL1), which lacks a
DELLA domain and is therefore not targeted for degradation in the
same manner.
A role attributed to submergence-induced SUB1A-1 is increased
maintenance of SLR1 and SLRL1. In lines possessing SUB1A-1,
levels of SLR1/SLRL1 mRNA and protein are enhanced by
submergence or treatment with ACC (Fukao & Bailey-Serres,
2008). New data suggest that the up-regulation of SLR1 protein
and mRNA of the GA catabolic gene GA2ox7 is mediated by
enhanced brassinosteroid (BR) biosynthesis in SUB1A-1 genotypes
(Schmitz et al., 2013). Submergence in the presence of the bioactive
BR brassinolide inhibits elongation growth, with greater inhibition
in SUB1A-1 genotypes. This indicates that shoot growth regulation
in submerged rice involves interplay between ethylene, BRs and
GA.
Accompanying the ethylene-driven GA-promoted elongation of
submerged shoots is the catabolism of starch and soluble sugars
(Fukao et al., 2006). This involves up-regulation of a-amylases in
the leaf mesophyll which break down starch to sugars, for
production of ATP by oxidative phosphorylation when O2 is
present or anaerobic metabolism if O2 is limiting. Submerged rice
leaves rapidly deplete the available starch with concomitant
increases in amino acids, TCA intermediates and fermentation
end-products (Barding et al., 2012, 2013). Genotypes with
submergence-inducible or constitutively expressed SUB1A-1
induce lower levels of leaf a-AMYLASE transcripts (Fukao et al.,
2006; Fukao & Bailey-Serres, 2008). Consistent with the observations that the LOQS involves less mobilization of hydrolysable
carbon, SUB1A-1 lines restrict the rate and extent of starch
hydrolysis and accumulate lower concentrations of ethanol, lactate
and alanine as well as amino acid metabolic end-products (Fukao
et al., 2006; Barding et al., 2012, 2013). This restriction on
metabolism probably occurs at the level of mobilization of carbon
reserves, as SUB1A-1 genotypes accumulate higher levels of PCD
and ADH transcripts and enzymes under submergence.
The LOQS of Sub1 rice extends beyond carbohydrate conservation. As noted in several studies, ethylene-driven declines in leaf
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chlorophyll content occur more rapidly in genotypes lacking
SUB1A-1 (Ella et al., 2003; Fukao et al., 2006; Winkel et al., 2014).
Chlorophyll breakdown also occurs when rice plants are left in the
dark for extended periods, a situation that can occur as a result of
submergence in turbid waters. Remarkably, SUB1A-1 transcript
levels rose over 100-fold in leaves after 1 d of anticipated darkness
(Fukao et al., 2012), although levels of this transcript did not rise
under a standard diurnal regime (Pe~
na-Castro et al., 2011). The
dampening of dark-induced chlorophyll catabolism and a more
rapid recovery of photosynthetic activity upon re-illumination were
correlated with lower induction of transcripts associated with
chlorophyll catabolism (Fukao et al., 2012). Transcripts of DELAY
OF THE ONSET OF SENESCENCE (DOS), which encodes a zincfinger TF that negatively regulates chlorophyll catabolism, were also
significantly elevated in SUB1A-1, further indicating that SUB1A
activity somehow dampens carbon and nitrogen mobilization
under energy-limiting conditions (darkness and submergence).
Studies of flooding responses of Rumex and Lotus species indicate
that quiescence and escape are not mutually exclusive. In Lotus
tenuis, shoots elongate upon partial submergence but arrest growth
when completely submerged, apparently switching from LOES to
LOQS (Manzur et al., 2009). This is associated with an elevated
shoot porosity and limited consumption of soluble carbohydrates
in the shoot/root crown. Lethal Time 50 (LT50) analyses suggest
that fully submerged R. palustris survives submergence in darkness
just as well as its ‘quiescent’ relative R. acetosa (van Veen et al.,
2014). Interestingly, anoxia survival was improved when
R. palustris plants were pretreated with ethylene, whereas that of
R. acetosa was not (van Veen et al., 2013). These observations
indicate that the capacity for a LOES does not preclude the ability
to invoke the LOQS. The petiole-specific activation of the signaling
machinery previously associated with shade avoidance, independent of phytochromes, may underlie the regional-specific changes
that manifest underwater elongation, reminiscent of the behavior
of stem internode regions in deepwater rice. Contrasting adaptation strategies are also illustrated by tree species in the Amazonian
floodplains, which can manage high metabolic levels that sustain
growth during submergence (Herrera, 2013; Kreuzwieser &
Rennenberg, 2014). In conclusion, although the LOES may result
in a net consumption of carbohydrates in specific cells, it might be
combined with LOQS determined by a threshold of O2 or energy
deficiency.
VII. After the deluge
Flooding events are frequently transient, as a result of agricultural
management of floodwaters or natural drainage. Key to an effective
waterlogging or submergence survival strategy is the ability to
remain reproductively viable. The LOES enables flowering and
fruiting to occur above the air–water interface. For plants with the
LOQS, fitness requires the capacity to quickly resume growth,
flower and set seeds after the inundation subsides. For either
survival strategy, several factors are to be considered: control of
ROS formed upon reoxygenation; return to homeostasis including
recovery of photosynthetic activity and prevention of desiccation;
and progression of development to reproduction.
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Studies in an array of species and O2 conditions have noted
elevation of transcripts associated with response to oxidative stress,
emphasizing their importance (Branco-Price et al., 2008; Blokhina
et al., 2014). There are also many demonstrated instances of ROS
production or damage in response to reoxygenation (reviewed by
Fukao & Bailey-Serres, 2004; Bailey-Serres & Chang, 2005;
Blokhina & Fagerstedt, 2010). It is hypothesized that, as cells
transit from hypoxia to normoxia, there is a burst in superoxide
production at complex III (cytochrome bc1) of the mitochondrial
electron transport chain, as a result of a lag in reactivation of
complex IV (cytochrome c oxidase) (Santosa et al., 2007). A
deficiency in antioxidants or antioxidant enzymes upon reoxygenation would lead to damage of cellular membranes, which could
impact cell integrity. Intriguingly, the burst in ROS emanating
from mitochondria upon both O2 deprivation and reoxygenation
promotes the transient activation of MAP kinases that play key
signaling roles in abiotic and biotic stress responses in A. thaliana
(Chang et al., 2012). Evidence of the importance of ROS
management during reoxygenation comes from the finding that
Sub1 rice minimizes ROS accumulation and leaf water loss during
desubmergence recovery (Fukao et al., 2011). Sub1 lines have
higher levels of mRNAs associated with limitation of ROS
accumulation before and during the recovery phase (Jung et al.,
2010; Mustroph et al., 2010; Fukao et al., 2011).
The transition from O2-deprived to O2-replete conditions will
undoubtedly result in a rapid change in cellular redox status. Our
understanding of low-O2 sensing mediated by the Arg/N-end rule
pathway indicates that ERF-VII N-terminal cysteine oxidation
enhanced by PCO1/2 (Weits et al., 2014) would result in rapid
degradation of the TF, thereby switching off the synthesis of
mRNAs encoding key enzymes of anaerobic metabolism. Reactive
cysteines may be relevant to other rapid adjustments upon changes
in O2 availability and redox status upon reaeration. These could
include regulation of other TFs, release of mRNAs that are
sequestered from the translational apparatus and regulation of
membrane transporters.
Desubmergence or reaeration of plants results in significant
changes in gene transcript accumulation (e.g. studies by BrancoPrice et al., 2008; Tamang et al., 2014; Tsai et al., 2014). It is well
established that ethylene evolution is enhanced in a species-specific
way upon desubmergence (Voesenek et al., 2003). In A. thaliana
seedlings, reaeration promotes accumulation of transcripts associated with ethylene production (Branco-Price et al., 2008); moreover, ethylene-insensitive mutants (ein2-5 and ein3 eil1) are
dysfunctional in up-regulation of many functional classes of gene
during reoxygenation (Tsai et al., 2014). This suggests that
ethylene signaling plays a role during stress recovery, perhaps
independent of the demise of ERF-VIIs.
Often submergence and waterlogging reduce maximum photosystem II (PSII) quantum efficiency (Kreuzwieser & Rennenberg,
2014), albeit the presence of leaf gas films on submerged leaves can
limit this constraint (Winkel et al., 2014). An underlying cause is
the degradation of chlorophyll, which as mentioned is less
pronounced during submergence or extended darkness in Sub1
rice (Fukao et al., 2006, 2012). Other studies have recognized a
correlation between submergence tolerance and the ability to
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rapidly recover photosynthesis (Luo et al., 2009, 2011), including
the ability of some species to retain functional PSII complexes even
after prolonged periods of submergence in darkness (i.e. certain
species endemic to Amazonian river floodplains; reviewed by
Parolin, 2008; Herrera, 2013). A better understanding of the
mechanisms associated with chloroplast maintenance, modifications, or turnover in flooded tissues is needed.
VIII. Perspective
Examination of species endemic to environments that experience
various flooding regimes as well as the semiaquatic crop rice has
identified plastic developmental, physiological and molecular
mechanisms that benefit survival. The combined recognition of a
low-O2 homeostasis mechanism that controls anaerobic metabolism in A. thaliana and key molecular and physiological processes
from rice and wild species such as R. palustris provides knowledge
that might be deployed to improve flooding survival of key crops.
Here we propose two scenarios for ‘waterproofing’ plants.
The first scenario involves the manipulation of ERF-VII
activity and turnover. The conservation of ERF-VIIs and Arg/Nend rule pathway (MetAP, ATE1/2, PRT6 and PCO1/2), HB1
and HRA1 genes in diverse land plants indicates that the low-O2
regulation of hypoxia-responsive genes is highly conserved.
Moreover, the strong overlap in transcriptome responses to
flooding/hypoxia across species and at multiple developmental
stages (Mustroph et al., 2010; Narsai et al., 2011; van Veen et al.,
2013) suggests the manipulation of this core module is an avenue
for improvement of flooding survival. The submergence resilience
of A. thaliana genotypes with modified ERF-VII turnover,
resulting from manipulation of the N-termini of the ERF-VIIs or
the Arg/N-end rule pathway components (Gibbs et al., 2011;
Licausi et al., 2011; Giuntoli et al., 2014; Weits et al., 2014),
strongly indicates that this module can be used to enable LOQS.
The results in A. thaliana are promising; approximately a
doubling of LT50 was observed in prt6 mutants compared with
wild type when submerged in darkness (R. Sasidharan, pers.
comm.). Future translation of this knowledge to crops requires
consideration of the native ERF-VIIs, the location and timing of
their expression, proteins that control their activity, and direct
gene targets. This need is exemplified by two recent findings: first,
that HRA1 limits the activity of RAP2.12 (Giuntoli et al., 2014)
and, secondly, that the DELLAs Gibberellin insensitive (GAI)
and Repressor of ga1-3 (RGA) bind RAP2.3 to limit its binding
to target gene sequences (Marın-de la Rosa et al., 2014).
The second scenario involves the identification and transfer of
survival solutions between cultivars and species. Within-species
transfer is elegantly demonstrated in rice with the SUB1A and SK1/
2 genes. The submergence tolerance regulator SUB1A-1 influences
anaerobic metabolism but extends its impact to GA-mediated
elongation growth. The remarkably antithetical regulation of GA
biosynthesis and the apparent responsiveness associated with SK1/
SK2 of deepwater elongating rice emphasize that carbon-consumptive metabolism can be pushed to the other extreme to enable
survival. Although the heterologous constitutive expression of
SUB1A-1 in A. thaliana did not yield submergence-tolerant plants,
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Review 69
the transgenics displayed increased GA-responsiveness and
increased ABA responsiveness (Pe~
na-Castro et al., 2011), similar
to SUB1A-1 overexpression lines of rice (Fukao & Bailey-Serres,
2008). There are other demonstrations of the value of the betweenspecies translation approach, as illustrated by waterlogging-tolerant
Hordeum marinum (wild sea barley), a relative of wheat (T. aestivum). Hordeum marinum is characterized by higher root porosity
and a stronger ROL barrier in the basal zones of ARs compared with
wheat. Hordeum marinum–wheat amphiploids display higher root
porosities and an effective ROL barrier, demonstrating the
successful transfer of waterlogging tolerance traits to wheat (Malik
et al., 2010). Although details of the relevant molecular and
developmental mechanisms remain uncharacterized, this example
illustrates successful transfer of flood tolerance from wild relatives
to crops cultivars. Continued identification of genetic diversity in
flooding survival traits – acting at seed, seedling and reproductive
stages and for a range of flooding regimes – is essential.
We advocate that a ‘learn from nature’ approach provides
potential to identify and mobilize additional genes and pathways
that provide effective survival strategies. These may be those lost
during crop domestication or present only in species adapted to
specific ecological niches. As already demonstrated, next-generation sequencing technologies coupled with physiological studies
can be applied to wild species to glean insights into mechanisms
not present in model species. The advancement of genomic
methodologies and genome editing technologies provide exciting
opportunities and the promise that insurance against unanticipated flooding can be effectively added to crops to improve yield
stability.
Acknowledgements
The authors grateful acknowledge Utrecht University, The Center
for Biosystems Genomics (CBSG2012), University of California,
Riverside, Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)(Grant nos. 819.01.006 and 863.12.013), the US
National Science Foundation MCB-1021969 (IOS 1121626 and
IOS-1238243), and the US Department of Agriculture, National
Institute of Food and Agriculture – Agriculture and Food Research
Initiative (Grant no. 2011–04015) for financial support. Hans van
Veen, Rashmi Sasidharan and Travis Lee are acknowledged for
scientific advice while writing this review. We apologize that it was
not possible to cite many recent papers in the flooding field because
of space constraints.
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